Advertisement

Mycorrhiza

, Volume 21, Issue 5, pp 375–391 | Cite as

Effects of twice-ambient carbon dioxide and nitrogen amendment on biomass, nutrient contents and carbon costs of Norway spruce seedlings as influenced by mycorrhization with Piloderma croceum and Tomentellopsis submollis

  • Rosemarie Barbara Weigt
  • Stefan Raidl
  • Rita Verma
  • Hermann Rodenkirchen
  • Axel Göttlein
  • Reinhard Agerer
Original Paper

Abstract

Elevated tropospheric CO2 concentrations may increase plant carbon fixation. In ectomycorrhizal trees, a considerable portion of the synthesized carbohydrates can be used to support the mutualistic fungal root partner which in turn can benefit the tree by increased nutrient supply. In this study, Norway spruce seedlings were inoculated with either Piloderma croceum (medium distance “fringe” exploration type) or Tomentellopsis submollis (medium distance “smooth” exploration type). We studied the impact of either species regarding fungal biomass production, seedling biomass, nutrient status and nutrient use efficiency in rhizotrons under ambient and twice-ambient CO2 concentrations. A subset was amended with ammonium nitrate to prevent nitrogen imbalances expected under growth promotion by elevated CO2. The two fungal species exhibited considerably different influences on growth, biomass allocation as well as nutrient uptake of spruce seedlings. P. croceum increased nutrient supply and promoted plant growth more strongly than T. submollis despite considerably higher carbon costs. In contrast, seedlings with T. submollis showed higher nutrient use efficiency, i.e. produced plant biomass per received unit of nutrient, particularly for P, K and Mg, thereby promoting shoot growth and reducing the root/shoot ratio. Under the given low soil nutrient availability, P. croceum proved to be a more favourable fungal partner for seedling development than T. submollis. Additionally, plant internal allocation of nutrients was differently influenced by the two ECM fungal species, particularly evident for P in shoots and for Ca in roots. Despite slightly increased ECM length and biomass production, neither of the two species had increased its capacity of nutrient uptake in proportion to the rise of CO2. This lead to imbalances in nutritional status with reduced nutrient concentrations, particularly in seedlings with P. croceum. The beneficial effect of P. croceum thus diminished, although the nutrient status of its host plants was still above that of plants with T. submollis. We conclude that the imbalances of nutrient status in response to elevated CO2 at early stages of plant development are likely to prove particularly severe at nutrient-poor soils as the increased growth of ECM cannot cover the enhanced nutrient demand. Hyphal length and biomass per unit of ectomycorrhizal length as determined for the first time for P. croceum amounted to 6.9 m cm−1 and 6.0 μg cm−1, respectively, across all treatments.

Keywords

Elevated CO2 Ectomycorrhiza Mycelium Fungal biomass Nitrogen Phosphate Potassium Magnesium Calcium Macronutrients Micronutients Nutrient use efficiency Rhizotrons Piloderma croceum Tomentellopsis submollis Picea abies 

Notes

Acknowledgements

This work was funded by the German Research Foundation (DFG) as part of the interdisciplinary research program “SFB 607—Growth and Parasite Defense” (sub-projects B7 and B10). We appreciate very much the help provided by our technicians E. Marksteiner and C. Bubenzer-Hange. The Department of Environmental Engineering at the German Research Center for Environmental Health is kindly acknowledged for providing the greenhouse facilities.

References

  1. Agerer R (1987–2008) Colour atlas of ectomycorrhizae. 1st–14th del. Einhorn, Schwäbisch GmündGoogle Scholar
  2. Agerer R (1998) Tomentellopsis submollis. In: Agerer R (ed) Colour atlas of ectomycorrhizae, plate 138. Einhorn, Schwäbisch GmündGoogle Scholar
  3. Agerer R (1999) Never change a functionally successful principle: the evolution of Boletales s. l. (Hymenomycetes, Basidiomycota) as seen from below-ground features. Sendtnera 6:5–91Google Scholar
  4. Agerer R (2001) Exploration types of ectomycorrhizae. A proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114CrossRefGoogle Scholar
  5. Agerer R (2007) Diversity of ectomycorrhizae as seen from below and above ground: the exploration types. Z Mykol 73:61–88Google Scholar
  6. Agerer R, Rambold G (1998) DEEMY, a DELTA-based information system for characterization and determination of ectomtcorrhizae, version 1.1. Mycology Section, Institute for Systematic Botany, University of München, MünchenGoogle Scholar
  7. Agerer R, Göttlein A (2003) Correlations between projection area of ectomycorrhizae and H2O extractable nutrients in organic soil layers. Mycol Prog 2:45–52CrossRefGoogle Scholar
  8. Agerer R, Raidl S (2004) Distance related half-quantitative estimation of the emanating ectomycorrhizal mycelia of Cortinarius obtusus and Tylospora asterophora. Mycological Progress 3:57–64CrossRefGoogle Scholar
  9. Agerer R, Rambold G (2004–2009 [first posted on 2004-06-01; most recent update: 2009-01-26]). DEEMY—an information system for characterization and determination of ectomycorrhizae. MünchenGoogle Scholar
  10. Alberton O, Kuyper TW (2009) Ectomycorrhizal fungi associated with Pinus sylvestris seedlings respond differently to increased carbon and nitrogen availability: implications for ecosystem responses to global change. Glob Chang Biol 15(1):166–175CrossRefGoogle Scholar
  11. Alberton O, Kuyper TW, Gorissen A (2005) Taking mycocentrism seriously: mycorrhizal fungal and plant responses to elevated CO2. New Phytol 167:859–868CrossRefPubMedGoogle Scholar
  12. Alberton O, Kuyper TW, Gorisson A (2007) Competition for nitrogen between Pinus sylvestris and ectomycorrhizal fungi generates potential for negative feedback under elevated CO2. Plant Soil 296:159–172CrossRefGoogle Scholar
  13. Alexander IJ, Fairley RJ (1983) Effects of N fertilization on populations of fine roots and mycorrhizas in spruce humus. Plant Soil 71:49–54CrossRefGoogle Scholar
  14. Allen MF (1991) The ecology of mycorrhizae. Cambridge University Press, CambridgeGoogle Scholar
  15. Anderson IC, Cairney JWG (2007) Ectomycorrhizal fungi: exploring the mycelial frontier. FEMS Microbiol Rev 31(4):388–406CrossRefPubMedGoogle Scholar
  16. Arnebrant K, Söderström B (1992) Effects of fertilizer treatments on ectomycorrhizal colonization potential in two Scots pine forests in Sweden. For Ecol Manag 53:77–89CrossRefGoogle Scholar
  17. Arocena JM, Glowa KR, Masicotte HB (2001) Calcium-rich hypha encrustations on Piloderma. Mycorrhiza 10:209–215CrossRefGoogle Scholar
  18. Bååth E, Söderström B (1979) Fungal biomass and fungal immobilization of plant nutrients in Swedish coniferous forest soils. Rev Ecol Biol Soil 16:477–489Google Scholar
  19. Bakken LR, Olsen RA (1983) Buoyant densities and dry-matter contents of microorganisms: conversion of a measured biovolume into biomass. Appl Environ Microbiol 45:1188–1195PubMedPubMedCentralGoogle Scholar
  20. Bidartondo MI, Ek H, Wallander H, Söderström B (2001) Do nutrient additions alter carbon sink strength of ectomycorrhizal fungi? New Phytol 151:543–550CrossRefGoogle Scholar
  21. BMVEL (2005) Handbuch Forstliche Analytik. Bundesministerium f. Verbraucherschutz, Ernährung und Landwirtschaft, BonnGoogle Scholar
  22. Brand F (1991a) Ektomykorrhizen an Fagus sylvatica. Charakterisierung und Identifizierung, ökologische Kennzeichnung und unsterile Kultivierung. Libri botanici vol 2, IHW, Eching, pp 1–229Google Scholar
  23. Brand F (1991b) Piloderma croceum. In: Agerer R (ed) Colour atlas of ectomycorrhizae, plate 62. Einhorn, Schwäbisch GmündGoogle Scholar
  24. Bücking H, Heyser W (1999) Elemental composition and function of polyphosphates in ectomycorrhizal fungi—an X-ray microanalytical study. Mycol Res 103:31–39CrossRefGoogle Scholar
  25. Cairney JWG, Jennings DH, Agerer R (1991) The nomenclature of fungal multi-hyphal linear aggregates. Cryptogam Bot 2(3):246–251Google Scholar
  26. Chapin FS III (1980) The mineral nutrition of wild plants. Ann Rev Ecol Syst 11:233–260CrossRefGoogle Scholar
  27. Colpaert JV, van Tichelen KK (1996) Mycorrhizas and environmental stress. In: Frankland JC, Magan N, Gadd GM (eds) Fungi and environmental change. Symposium of the British Mycological Society. Cambridge University Press, Cambridge, pp 109–128Google Scholar
  28. Colpaert JV, van Assche JA, Luijtens K (1992) The growth of the extramatrical mycelium of ectomycorrhizal fungi and the growth responses of Pinus sylvestris L. New Phytol 120:127–135CrossRefGoogle Scholar
  29. Conroy JP, Milham PJ, Bevege DI, Barlow EWR (1990) Influence of phosphorus deficiency on the growth response of four families of Pinus radiata seedlings to CO2-enriched atmospheres. For Ecol Manag 30:175–188CrossRefGoogle Scholar
  30. Duddridge JA, Malibari A, Read DJ (1980) Structure and function of mycorrhizal rhizomorphs with special reference to their role in water transport. Nature (London) 287:834–836CrossRefGoogle Scholar
  31. Ek H (1997) The influence of nitrogen fertilization on the carbon economy of Paxillus inolutus in ectomycorrhizal association with Betula pendula. New Phytol 135:133–142CrossRefGoogle Scholar
  32. Ericsson T (1995) Growth and shoot: root ratio of seedlings in relation to nutrient availability. Plant Soil 168–169:205–214CrossRefGoogle Scholar
  33. Frankland JC, Lindley AK, Swift MJ (1978) A comparison of two methods for the estimation of mycelial biomass in leaf litter. Soil Biol Biochem 10:323–333CrossRefGoogle Scholar
  34. Fransson PMA, Taylor AFS, Finlay RD (2000) Effects of continuous optimal fertilization on belowground ectomycorrhizal community structure in a Norway spruce forest. Tree Physiol 20:599–606CrossRefPubMedGoogle Scholar
  35. Fransson PM, Taylor AF, Finlay RD (2005) Mycelial production, spread and root colonisation by the ectomycorrhizal fungi Hebeloma crustuliniforme and Paxillus involutus under elevated atmospheric CO2. Mycorrhiza 15:25–31CrossRefPubMedGoogle Scholar
  36. Franz F (1994) Ektomykorrhizen der Fichte: Identifizierung, Ultrastruktur und Miroelementanalyse (EELS, ESI). Diss Univ BayreuthGoogle Scholar
  37. Garcia MO, Ovasapyan T, Greas M, Treseder KK (2008) Mycorrhizal dynamics under elevated CO2 and nitrogen fertilization in a warm temperate forest. Plant Soil 303:301–310CrossRefGoogle Scholar
  38. Godbold DL, Berntson GM (1997) Elevated atmospheric CO2 concentration changes ectomycorrhizal morphotype assemblages in Betula papyrifera. Tree Physiol 17:347–350CrossRefPubMedGoogle Scholar
  39. Godbold DL, Berntson GM, Bazzaz FA (1997) Growth and mycorrhizal colonization of three North American tree species under elevated CO2. New Phytol 137:433–440CrossRefGoogle Scholar
  40. Godbold DL, Hoosbeek MR, Lukac M, Cotrufo MF, Janssens IA, Ceulemans R, Polle A, Velthorst EJ, Scarascia-Mugnozza G, De Angelis P, Miglietta F, Peressotti A (2006) Mycorrhizal hyphal turnover as a dominant process for carbon input into soil organic matter. Plant Soil 281:15–24CrossRefGoogle Scholar
  41. Gorissen A, Kuyper TW (2000) Fungal species-specific responses of ectomycorrhizal Scots pine (Pinus sylvestris) to elevated CO2. New Phytol 146:163–168CrossRefGoogle Scholar
  42. Handa T, Hagedorn F, Hättenschwiler S (2008) No stimulation in root production in response to 4 years of in situ CO2 enrichment at the Swiss treeline. Funct Ecol 22:348–358CrossRefGoogle Scholar
  43. Haug I, Pritsch K (1992) Ectomycorrhizal types of spruce (Picea abies (L.) Karst.) in the Black Forest. A microscopical atlas. Kernforschungszentrum Karlsruhe, PEF-Ber, pp 1–89Google Scholar
  44. Högberg MN, Högberg P (2002) Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytol 154:791–795CrossRefGoogle Scholar
  45. Holmgren PK, Holmgren NH, Barnett LC (1990) Index herbariorum. Part I. Herbaria of the world. 8th edn. [Regnum Vegetabile No. 120] New York Botanical Garden, New York (http://www.nybg.org/bsci/ih/ih.html)
  46. Ineichen K, Wiemken V, Wiemken A (1995) Shoots, roots and ectomycorrhiza formation of pine seedlings at elevated atmospheric carbon dioxide. Plant Cell Environ 18:703–707CrossRefGoogle Scholar
  47. IPCC (2007) Zusammenfassung für politische Entscheidungsträger. In: Klimaänderung 2007: Wissenschaftliche Grundlagen. Beitrag der Arbeitsgruppe I zum Vierten Sachstandsbericht des Zwischenstaatlichen Ausschusses für Klimaänderung (IPCC), Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL, eds, Cambridge University Press, Cambridge, United Kingdom und New York, NY, USA. Deutsche Übersetzung durch ProClim-, österreichisches Umweltbundesamt, deutsche IPCC-Koordinationsstelle, Bern/Wien/Berlin, 2007Google Scholar
  48. Iversen CM (2010) Digging deeper: fine-root responses to rising atmospheric [CO2] concentration in forest ecosystems. New Phytol 186:346–357CrossRefPubMedGoogle Scholar
  49. Janssens I, Crookshanks M, Taylor G, Ceulemans R (1998) Elevated atmospheric CO2 increases fine root production, respiration, rhizosphere respiration and soil CO2 efflux in Scots pine seedlings. Glob Chang Biol 4:871–878CrossRefGoogle Scholar
  50. Jentschke G, Brandes B, Kuhn AJ, Schröder WH, Godbold DL (2001) Interdependence of phosphorus, nitrogen, potassium and magnesium translocation by the ectomycorrhizal fungus Paxillus involutus. New Phytol 149:327–337CrossRefGoogle Scholar
  51. Johnson DW, Ball T, Walker RF (1995) Effects of elevated CO2 and nitrogen on nutrient uptake in ponderosa pine seedlings. Plant Soil 168(169):535–545CrossRefGoogle Scholar
  52. Johnson MG, Rygiewicz PT, Tingey DT, Phillips DL (2006) Elevated CO2 and elavated temerature have no effect on Douglas-fir fine-root dynamics in nitrogen-poor soil. New Phytol 170:345–356CrossRefPubMedGoogle Scholar
  53. Jones MD, Durall DM, Tinker PB (1990) Phosphorus relationship and production of extramatrical hyphae by two types of willow ectomycorrhizas at different soil phosphorus levels. New Phytol 115(2):259–268CrossRefGoogle Scholar
  54. Jones MD, Durall DM, Tinker PB (1991) Fluxes of carbon and phosphorus between symbionts in willow ectomycorrhizas and their changes with time. New Phytol 119:99–106CrossRefGoogle Scholar
  55. Kammerbauer H, Agerer R, Sandermann H (1989) Studies on ectomycorrhiza XXII. Mycorrhizal rhizomorphs of Thelephora terrestris and Pisolithus tinctorius in association with Norway spruce (Picea abies): formation in vitro and translocation of phosphate. Trees 3:78–84CrossRefGoogle Scholar
  56. Kasurinen A, Helmisaari H-S, Holopainen T (1999) The influence of elevated CO2 and O3 on fine roots and mycorrhizas of naturally growing young Scots pine trees during three exposure years. Glob Chang Biol 5:771–780CrossRefGoogle Scholar
  57. King JS, Hanson PJ, Bernhardt E, DeAngelis P, Norby RJ, Pregitzer KS (2004) A multiyear synthesis of soil respiration responses to elevated atmospheric CO2 from four forest FACE experiments. Glob Chang Biol 10:1027–1042CrossRefGoogle Scholar
  58. Koch N, Andersen CP, Raidl S, Agerer R, Matyssek R, Grams TEE (2007) Temperature–respiration relationships differ in mycorrhizal and non-mycorrhizal root systems of Picea abies (L.) Karst. Plant Biol 9:545–549CrossRefPubMedGoogle Scholar
  59. Köljalg U, Tammi H, Timonen S, Agerer R, Sen R (2001) ITS rDNA sequence-based positioning of pink-type ectomycorrhizas and Tomentellopsis species from boreal and temperate forests. Mycol Progr 1:81–92CrossRefGoogle Scholar
  60. Kunzweiler K, Kottke I (1986) Quantifizierung von Mycel im Boden. In: Einsele G (ed) Das landschaftsökologische Forschungsprojekt Naturpark Schönbuch, DFG-Forschungsbericht, VHV Weinheim, pp 429–441Google Scholar
  61. Leake J, Johnson D, Donelly D, Muckle G, Boddy L, Read D (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystems. Can J Bot 82:1016–1045CrossRefGoogle Scholar
  62. Lewis JD, Strain BR (1996) The role of mycorrhizas in the response of Pinus taeda seedlings to elevated CO2. New Phytol 133:431–443CrossRefGoogle Scholar
  63. Lewis JD, Thomas RB, Strain BR (1994) Effect of elevated CO2 on mycorrhizal colonization of loblolly pine (Pinus taeda L.) seedlings. Plant and Soil 165:81–88CrossRefGoogle Scholar
  64. Marschner H, Kirkby E, Cakmak I (1996) Effect of mineral nutritional status on shoot–root partitioning of photoassimilates and cycling of mineral nutrients. J Exp Bot 47:1255–1263CrossRefPubMedGoogle Scholar
  65. Marx DH (1969) The influence of ectotrophic mycorrhizal fungi on the resistance of pine roots to pathogenic infections: I. Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology 59:153–163Google Scholar
  66. Matuszkiewicz W (1962) Zur Systematik der natürlichen Kiefernwälder des mittel- und osteuropäischen Flachlandes. Mitt. flor.-soz. Arbeitsgem., Stolzenau/Weser, N.F 9:145–186Google Scholar
  67. McCarthy HR, Oren R, Johnsen KH, Gallet-Budynek A, Pritchard SG, Cook CW, LaDeau SL, Jackson RB, Finzi AC (2010) Re-assessment of plant carbon dynamics at the Duke free-air CO2 enrichment site: interactions of atmospheric [CO2] with nitrogen and water availability over stand development. New Phytol 185:514–528CrossRefPubMedGoogle Scholar
  68. Millard P, Sommerkorn M, Grelet GA (2007) Environmental change and carbon limitation in trees: a biochemical, ecophysiological and ecosystem appraisal. New Phytol 175:11–28CrossRefPubMedGoogle Scholar
  69. Moorhead DL, Linkins AE (1997) Elevated CO2 alters belowground exoenzyme activities in tussock tundra. Plant Soil 189:321–329CrossRefGoogle Scholar
  70. Mousseau M, Saugier B (1992) The direct effect of increased CO2 on gas exchange and growth of forest tree species. J Exp Bot 43:1121–1130CrossRefGoogle Scholar
  71. Nakayama FS, Hulukab G, Kimballa BA, Lewinc KF, Nagyc J, Hendrey GR (1994) Soil carbon dioxide fluxes in natural and CO2-enriched systems. Agric For Meteorol 70:131–140CrossRefGoogle Scholar
  72. Nilsson LO (2004) External mycelia of mycorrhizal fungi. Ph.D. thesis, Department of Ecology, Lund University, SwedenGoogle Scholar
  73. Norby JN, O’Neill EG, Luxmoore RJ (1986) Effects of atmospheric CO2 enrichment on the growth and mineral nutrition of Quercus alba seedlings in nutrient-poor soil. Plant Physiol 82:83–89CrossRefPubMedPubMedCentralGoogle Scholar
  74. Norby RJ, O’Neill EG, Hood WG, Luxmoore RJ (1987) Carbon allocation, root exudation and mycorrhizal colonization of Pinus echinata seedlings grown under CO2 enrichment. Tree Physiol 3:203–210CrossRefPubMedGoogle Scholar
  75. Norby RJ, Ledford J, Reilly CD, Miller NE, O’Neill EG (2004) Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment. Proc Natl Acad Sci 101:9689–9693CrossRefPubMedPubMedCentralGoogle Scholar
  76. O’Neill EG (1994) Responses of soil biota to elevated atmospheric carbon dioxide. Plant Soil 165:55–65CrossRefGoogle Scholar
  77. O’Neill EG, Luxmoore RJ, Norby RJ (1987) Increases in mycorrhizal colonization and seedling growth in Pinus echinata and Quercus alba in an enriched CO2 atmosphere. Can J For Res 17:878–883CrossRefGoogle Scholar
  78. Parrent JL, Vilgalys R (2007) Biomass and compositional responses of ectomycorrhizal fungal hyphae to elevated CO2 and nitrogen fertilization. New Phytol 176:164–174CrossRefPubMedGoogle Scholar
  79. Parrent JL, Morris WF, Vilgalys R (2006) CO2-enrichment and nutrient availability alter ectomycorrhizal fungal communities. Ecology 87:2278–2287CrossRefPubMedGoogle Scholar
  80. Plassard C, Guérin-Laguette A, Véry A-A, Casarin V, Thibaud J-B (2002) Local measurements of nitrate and potassium fluxes along roots of maritime pine. Effects of ectomycorrhizal symbiosis. Plant Cell Environ 25:75–84CrossRefGoogle Scholar
  81. Pregitzer KS, Zak DR, Maziasz J, DeForest J, Curtis PS, Lussenhop J (2000) Interactive effects of atmospheric CO2 and soil-N availability on fine roots of Populus tremuloides. Ecol Appl 10:18–33Google Scholar
  82. Pritchard SG, Rogers HH, Davis M, van Santen E, Prior SA, Schlesinger WH (2001) The influence of elevated atmosphereic CO2 on fine root dynamics in an intact temperate forest. Glob Chang Biol 7:829–837CrossRefGoogle Scholar
  83. Pritchard SG, Strand AE, McCormack ML, Davis MA, Oren R (2008) Mycorrhizal and rhizomorph dynamics in a loblolly pine forest during 5 years of free-air-CO2-enrichment. Glob Chang Biol 14:1–13Google Scholar
  84. Raidl S (1997) Studien zur Ontogenie an Rhizomorphen von Ektomykorrhizen. Bibliotheca Mycologica, vol 169, Cramer, Braunschweig, pp 1–184Google Scholar
  85. Read DJ (1992) The mycorrhizal mycelium. In: Allen MF (ed) Mycorrhizal functioning. An integrative plant–fungal process. Chapman & Hall, New York, pp 102–133Google Scholar
  86. Rey A, Jarvis PG (1997) Growth response of young birch trees (Betula pendula Roth.) after four and a half years of CO2 exposure. Ann Bot 80:809–816CrossRefGoogle Scholar
  87. Rogers HH, Peterson CM, McCrimmon JN, Cure JD (1992) Response of plant roots to elevated atmospheric carbon dioxide. Plant Cell Environ 15:749–752CrossRefGoogle Scholar
  88. Rouhier H, Read DJ (1999) Plant and fungal responses to elevated atmospheric CO2 in mycorrhizal seedlings of Betula pendula. Environ Exp Bot 42:231–241CrossRefGoogle Scholar
  89. Rousseau JV, Sylvia DM, Fox AJ (1994) Contribution of ectomycorrhiza to the potential nutrient-absorbing surface of pine. New Phytol 128:639–644CrossRefGoogle Scholar
  90. Runion GB, Mitchell RJ, Rogers HH, Prior SA, Counts TK (1997) Effects of nitrogen and water limitation and elevated CO2 on ectomycorrhiza of longleaf pine. New Phytol 137:681–689CrossRefGoogle Scholar
  91. Rygiewicz PT, Andersen CP (1994) Mycorrhiza alter quality and quantity of carbon allocated below ground. Nature (London) 369:58–60CrossRefGoogle Scholar
  92. Rygiewicz PT, Johnson MG, Ganio LM, Tingey DT, Storm MJ (1997) Lifetime and temporal occurrence of ectomycorrhizae on ponderosa pine (Pinus ponderosa Laws.) seedlings grown under varied atmospheric CO2 and nitrogen levels. Plant Soil 189:275–287CrossRefGoogle Scholar
  93. Schlesinger WH, Andrews JA (2000) Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20CrossRefGoogle Scholar
  94. Schubert R, Raidl S, Funk R, Bahnweg G, Müller-Starck G, Agerer R (2003) Quantitative detection of agar-cultivated and rhizotron-grown Piloderma croceum Erikss. & Hjortst. by ITS-based fluorescent PCR. Mycorrhiza 13:159–165CrossRefPubMedGoogle Scholar
  95. Segmüller S, Rennenberg H (1994) Interactive effects of mycorrhization and elevated carbon dioxide on growth of young pedunculate oak (Quercus pedunculata L.) trees. Plant Soil 167:325–329CrossRefGoogle Scholar
  96. Simard SW, Durall DM, Jones MD (2002) Carbon and nutrient fluxes within and between mycorrhizal plants. In: van der Heijden MGA, Sanders IR (eds) Mycorrhizal ecology. Ecological studies 157. Springer, Berlin, pp 33–74Google Scholar
  97. Sittig U (1999) Zur saisonalen Dynamik von Ektomykorrhizen der Buche (Fagus sylvatica L.). Ber Forsch Waldökosyst 162:1–119Google Scholar
  98. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, San DiegoGoogle Scholar
  99. Söderström B, Read DJ (1987) Respiratory activity of intact and excised ectomycorrhizal mycelial systems growing in unsterilized soil. Soil Biol Biochem 19:231–236CrossRefGoogle Scholar
  100. Stalpers JA (1993) The aphyllophoraceous fungi I: kerys to the species of the Thelephorales. Studies in Mycology 35:1–168Google Scholar
  101. Thomas SM, Whitehead D, Reid JB, Cook FJ, Adams JA, Leckie AC (1999) Growth, loss, and vertical distribution of Pinus radiata fine roots growing at ambient and elevated CO2 concentration. Glob Chang Biol 5:07–121CrossRefGoogle Scholar
  102. Tingey DT, Phillips DL, Johnson MG (2000) Elevated CO2 and conifer roots: effects on growth, life span and turnover. New Phytol 147:87–103CrossRefGoogle Scholar
  103. Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355CrossRefGoogle Scholar
  104. Turnau K, Berger A, Loewe A, Einig W, Hampp R, Chalot M, Dizengremel P, Kottke I (2001) Carbon dioxide concentration and nitrogen input affect the C and N storage pools in Amanita muscariaPicea abies mycorrhizae. Tree Physiol 21:93–99CrossRefPubMedGoogle Scholar
  105. Walker RF, Geisinger DR, Johnson DW, Ball JT (1995) Interactive effects of atmospheric CO2 enrichment and soil N on growth and ectomycorrhizal colonization of ponderosa pine seedlings. Forest Sci 41:491–500Google Scholar
  106. Wang YP, Rey A, Jarvis PG (1998) Carbon balance of young birch trees grown in ambient and elevated atmospheric CO2 concentrations. Glob Chang Biol 4:797–807CrossRefGoogle Scholar
  107. Wiemken V, Laczko E, Ineichen K, Boller T (2001) Effects of elevated carbon dioxide and nitrogen fertilization on mycorrhizal fine roots and the soil microbial community in beech–spruce ecosystems on siliceous and calcareous soil. Microb Ecol 42:126–135PubMedGoogle Scholar
  108. Zak DR, Pregitzer KS, King JS, Holmes WE (2000) Elevated atmospheric CO2, fine roots and the response of soil microorganisms: a review and hypothesis. New Phytol 147:201–222CrossRefGoogle Scholar
  109. Zhu Y-G, Miller RM (2003) Carbon cycling by arbuscular mycorrhizal fungi in soil plant systems. Trends Plant Sci 8:407–409CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Rosemarie Barbara Weigt
    • 1
  • Stefan Raidl
    • 1
  • Rita Verma
    • 1
  • Hermann Rodenkirchen
    • 2
  • Axel Göttlein
    • 2
  • Reinhard Agerer
    • 1
  1. 1.Department of Biology I and GeoBio-Center (LMU), Division of Organismic Biology: MycologyLudwig-Maximilians-Universität MünchenMunichGermany
  2. 2.Department of Ecology and Ecosystem Management, Forest Nutrition and Water ResourcesTechnische Universität MünchenFreisingGermany

Personalised recommendations